Evolutionary trade-offs between beauvericin production and growth define divergent virulence strategies in Beauveria

Pathogen virulence is often attributed to toxin production, yet toxins are metabolically costly and may not universally enhance fitness. How such traits are maintained in natural populations remains poorly understood. Here we demonstrate that balancing selection maintains alternative virulence strategies in the insect-pathogenic fungus Beauveria.

A high-beauvericin (BEA)-producing strain (Beauveria amorpha) accumulated toxin during insect infection and inhibited gram-positive bacteria at physiologically relevant concentrations. On the other hand, a low-BEA-producing strain (Beauveria bassiana) exhibited accelerated growth, greater blastospore proliferation in hemolymph, and earlier cadaver sporulation. Despite large differences in toxin production, both strains achieved comparable host mortality, indicating that BEA is not the only determinant of pathogenicity. Instead, virulence was achieved through distinct strategies: a toxin strategy, characterized by secondary metabolite investment and antimicrobial activity, and a growth strategy, characterized by rapid within-host proliferation and competitive exclusion through biomass accumulation. BEA was not detected during endophytic colonization of soybean, indicating ecological context-dependent expression. Phylogenetic and transcriptional analyses revealed divergence in BEA-associated regulatory pathways, including elevated expression of the global regulator LaeA in the high-BEA lineage, suggesting evolutionary partitioning of metabolic investment.

These findings reveal an evolutionary trade-off between toxin production and growth that generates functionally equivalent but mechanistically distinct pathogenic outcomes. More broadly, our results provide empirical evidence that balancing selection can maintain alternative virulence strategies within a fungal lineage, offering a general framework for understanding the persistence of costly secondary metabolites in host-pathogen systems. © 2026 The Author(s). Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.